Abstract
The cultivable endophytic bacteria associated with two medicinal plants Hypericum perforatum L. and Ziziphora capitata L. contrasting with phytotoxic activity were investigated. The phytotoxic activity of plant extracts, and bacterial metabolites on seed germination and seedling growth of tomato were evaluated. In comparison to Z. capitata, the extract of H. perforatum contains a higher content of phenolic compounds. The crude extract of H. perforatum inhibited germination of seeds and seedling growth of tomato, whereas Z. capitata extracts only slightly reduced these parameters. Interestingly, almost half of the endophytes associated with H. perforatum had an inhibitory effect on plant growth, whereas rarely any plant inhibitory effect was found among isolates from Z. capitata. All bacterial isolates from Z. capitata were able to stimulate plant growth, by 35–80%. In contrast, only five isolates from H. perforatum caused significant improvement in plant growth (22–46%). The results showed that medicinal plants with higher phytotoxic activity were colonized with endophytic bacteria which inhibit plant growth and development. These findings indicate that plant phytochemical constituents and activity determine the physiological properties of their endophytes.
This is a preview of subscription content, log in via an institution to check access.
References
Ali ZH, Wang Q, Ruan X, Pan CD, Jiang DA (2010) Phenolics and plant allelopathy. Molecules 15(12):8933–8952. https://doi.org/10.3390/molecules15128933
Angelini LG, Carpanese G, Cioni PL, Morelli I, Macchia M, Flamini G (2003) Essential oils from Mediterranean Lamiaceae as weed germination inhibitors. J Agric Food Chem 51(21):6158–6164. https://doi.org/10.1021/jf0210728
Arora NK, Khare E, Singh S, Tewari S (2018) Phenetic, genetic diversity and symbiotic compatibility of rhizobial strains nodulating pigeon pea in Northern India. 3 Biotech 8(1):52. https://doi.org/10.1007/s13205-017-1074-1 (Epub 2018 Jan 4)
Baker S, Satish S (2013) Antimicrobial evaluation of fluorescent Pseudomonas sp. inhabiting medicinal plant Annona squamosa L. J Pure Appl Microbiol 7:1027–1033
Banowetz GM, Azevedo MD, Armstrong DJ, Halgren AB, Mills DI (2008) Germination-arrest factor (GAF): biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria. Biol Control 46:380–390. https://doi.org/10.1016/j.biocontrol.2008.04.016
Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37. https://doi.org/10.1016/j.copbio.2013.09.012
Brimecombe MJ, De Leij FAAM, Lynch JM (2007) Rhizodeposition and microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC Press, New York, pp 74–98
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196
Cho ST, Chang HH, Egamberdieva D, Kamilova F, Lugtenberg B, Kuo CH (2015) Genome analysis of Pseudomonas fluorescens PCL1751: a rhizobacterium that controls root diseases and alleviates salt stress for its plant host. PLoS ONE. https://doi.org/10.1371/journal.pone.0140231
Dall’Agnol R, Ferraz A, Bernardi AR, Albring D, Nör C, Sarmento L, Lamb L, Hass M, von Poser G, Schapoval EES (2003) Antimicrobial activity of some Hypericum species. Phytomedicine 10:511–516. https://doi.org/10.1078/094471103322331476
Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39:840–859. https://doi.org/10.1007/s10886-013-0306-z
Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013) Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by co-inoculation of rhizobium with root colonising Pseudomonas. Plant Soil 369(1):453–465. https://doi.org/10.1007/s11104-013-1586-3
Egamberdieva D, Li L, Lindström K, Räsänen L (2016) A synergistic interaction between salt tolerant Pseudomonas and Mezorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress. Appl Microb and Biotech 100(6):2829–2841. https://doi.org/10.1007/s00253-015-7147-3
Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G (2017a) Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol 8:199. https://doi.org/10.3389/fmicb.2017.00199
Egamberdieva D, Wirth S, Shurigin V, Hashem A, Abd_Allah EF (2017b) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8:1887. https://doi.org/10.3389/fmicb.2017.01887
Egamberdieva D, Hua M, Reckling M, Bellingrath-Kimura SD (2018) Environ Sustain. https://doi.org/10.1007/s42398-018-0010-6
Fritz D, Bernardi AP, Haas JS, Ascoli BM, Bordignon SAL, Braz PG (2007) Germination and growth inhibitory effects of Hypericum myrianthum and H. polyanthemum extracts on Lactuca sativa L. J Pharm 17(1):44–48. https://doi.org/10.1590/S0102-695X2007000100010
Goryluk A, Rekosz-Burlaqa H, Błaszczyk M (2009) Isolation and characterization of bacterial endophytes of Chelidonium majus. Pol J Microbiol 58:355–361
Hashem A, Abd_Allah EF, Alqarawi A, Al-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089. https://doi.org/10.3389/fmicb.2016.01089
Jbilou R, Amri H, Bouayad N, Ghailani N, Ennabili A, Sayah F (2008) Insecticidal effects of extracts of seven plant species on larval development, α-amylase activity and offspring production of Tribolium castaneum (Herbst) (Insecta: Coleoptera: Tenebrionidae). Bioresour Technol 99(5):959–964. https://doi.org/10.1016/j.biortech.2007.03.017
Ji HF, Li XJ, Zhang HY (2009) Natural products and drug discovery. Can thousands of years of ancient medical knowledge lead us to new and powerful drug combinations in the fight against cancer and dementia? EMBO Rep 10:194–200. https://doi.org/10.1038/embor.2009.12
Kai M, Effmert U, Piechulla B (2016) Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front Microbiol 7:108. https://doi.org/10.3389/fmicb.2016.00108
Köberl M, Ramadan EM, Adam M, Cardinale M, Hallmann J, Heuer H, Smalla K, Berg G (2013) Bacillus and Streptomyces were selected as broad-spectrum antagonists against soilborne pathogens from arid areas in Egypt. FEMS Microbiol Lett 342:168–178. https://doi.org/10.1111/1574-6968.12089
Kremer RJ, Souissi T (2001) Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol 43(3):182–186. https://doi.org/10.1007/s002840010284
Kumar G, Kanaujia N, Bafana A (2012) Functional and phylogenetic diversity of root-associated bacteria of Ajuga bracteosa in Kangra valley. Microb Res 167:220–225. https://doi.org/10.1016/j.micres.2011.09.001
Kusari S, Verma VC, Lamshoeft M, Spiteller M (2012) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28:1287–1294. https://doi.org/10.1007/s11274-011-0876-2
Ma YQ, Zhang W, Dong SQ, Ren XX, An Y, Lang M (2012) Induction of seed germination in Orobanche spp. by extracts of traditional Chinese medicinal herbs. Sci China Life Sci 55(3):250–260. https://doi.org/10.1007/s11427-012-4302-2
McPhail KL, Armstrong DJ, Azevedo MD, Banowetz GM, Mills DI (2010) 4-Formylaminooxyvinylglycine, an herbicidal germination-arrest factor from Pseudomonas rhizosphere bacteria. J Nat Prod 73:1853–1857. https://doi.org/10.1021/np1004856
Mehanni MM, Safwat MS (2010) Endophytes of medicinal plants. Acta Hort (ISHS) 854:31–39. https://doi.org/10.17660/ActaHortic.2010.854.3
Oztürk N, Tunçel M, Potoğlu-Erkara İ (2009) Phenolic compounds and antioxidant activities of some Hypericum ssp.: a comparative study with H. perforatum. Pharm Biol 47:120–127. https://doi.org/10.1080/13880200802437073
Puupponen-Pimiä R, Nohynek L, Meier C, Kähkönen M, Heinonen M, Hopia A, Oksman-Caldentey KM (2001) Antimicrobial properties of phenolic compounds from berries. J Appl Microbiol 90:494–507. https://doi.org/10.1046/j.1365-2672.2001.01271.x
Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Marostica Junior MR (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79. https://doi.org/10.1007/s13199-014-0273-3
Schmidt R, Cordovez V, de Boer W, Raaijmakers J, Garbeva P (2015) Volatile affairs in microbial interactions. ISME J 9(11):2329–2335
Slinkard K, Singleton VL (1977) Total phenol analyses: automation and comparison with manual methods. Am J Enol Vitic 28:49–55
Tabatabaei S, Ehsanzadeh P, Etesami H, Alikhani HA, Glick BR (2016) Indole-3-acetic acid (IAA) producing Pseudomonas isolates inhibit seed germination and α-amylase activity in durum wheat (Triticum turgidum L.). Span J Agric Res 14:1. https://doi.org/10.5424/sjar/2016141-8859
Tian S, Shi Y, Zhou X, Ge L, Upur H (2011) Total polyphenolic (flavonoids) content and antioxidant capacity of different Ziziphora clinopodioides Lam. extracts. Pharmacogn Mag 7:65–68. https://doi.org/10.4103/0973-1296.75904
Varsha S, Agrawal RC, Sonam P (2013) Phytochemical screening and determination of anti-bacterial and anti-oxidant potential of Glycyrrhiza glabra root extracts. J Environ Res Dev 7(4):1552–1558
Vashist H, Sharma D (2013) Pharmacognostical aspects of Glycyrrhiza glabra. Asian J Pharm Clin Res 6(4):55–59
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shurigin, V., Davranov, K., Wirth, S. et al. Medicinal plants with phytotoxic activity harbour endophytic bacteria with plant growth inhibitory properties. Environmental Sustainability 1, 209–215 (2018). https://doi.org/10.1007/s42398-018-0020-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42398-018-0020-4